Medicago truncatula DNF2 is a PI-PLC-XD-containing protein required for bacteroid persistence and prevention of nodule early senescence and defense-like reactions

New Phytologist

Volumn 197, Issue 4, 2013, Pages 1250-1261

  Bourcy, Marie ^a   Brocard, Lysiane ^a   Pislariu, Catalina I ^b   Cosson, Viviane ^a   Mergaert, Peter ^a   Tadege, Millon ^b   Mysore, Kirankumar S ^b   Udvardi, Michael K ^b   Gourion, Benjamin ^a   Ratet, Pascal ^a  

^a CNRS   (France)

^b PLANT BIOLOGY DIVISION   (United States)

Author keywords

Defense like reactions; Insertion mutant; Legume; Nitrogen fixation; Rhizobia; Senescence; Symbiosis; Symbiosome

Indexed keywords

VEGETABLE PROTEIN;

BACTERIUM; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ANALYSIS; LEGUME; MOLECULAR ANALYSIS; MUTATION; NITROGEN FIXATION; PLANT DEFENSE; PROTEIN; SENESCENCE; SYMBIOSIS;

ARTICLE; BARREL MEDIC; GENE INACTIVATION; GENETICS; METABOLISM; MICROBIOLOGY; NITROGEN FIXATION; PHENOTYPE; PHYSIOLOGY; SINORHIZOBIUM; SYMBIOSIS;

GENE KNOCKOUT TECHNIQUES; MEDICAGO TRUNCATULA; NITROGEN FIXATION; PHENOTYPE; PLANT PROTEINS; SINORHIZOBIUM; SYMBIOSIS;

BACTERIA (MICROORGANISMS); MEDICAGO TRUNCATULA; RHIZOBIACEAE; SINORHIZOBIUM MELILOTI;

EID: 84873242814     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12091     Document Type: Article

References (63)

1. Ardourel M, Demont N, Debelle F, Maillet F, de Billy F, Prome JC, Denarie J, Truchet G. 1994. Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6: 1357-1374.
2. Barsch A, Tellström V, Patschkowski T, Küster H, Niehaus K. 2006. Metabolite profiles of nodulated alfalfa plants indicate that distinct stages of nodule organogenesis are accompanied by global physiological adaptations. Molecular Plant-Microbe Interactions 19: 998-1013.
3. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T et al. 2008. A gene expression atlas of the model legume Medicago truncatula. Plant Journal 55: 504-513.
4. Boivin C, Camut S, Malpica CA, Truchet G, Rosenberg C. 1990. Rhizobium meliloti genes encoding catabolism of trigonelline are induced under symbiotic conditions. Plant Cell 2: 1157-1170.
5. Brocard L, Schultze M, Kondorosi A, Ratet P. 2006. T-DNA mutagenesis in the model plant Medicago truncatula: is it efficient enough for legume molecular genetics? CAB reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 1: 1-7.
6. Canonne J, Froidure-Nicolas S, Rivas S. 2011. Phospholipases in action during plant defense signaling. Plant Signaling & Behaviour 6: 13-18.
7. Cebolla A, Vinardell JM, Kiss E, Olah B, Roudier F, Kondorosi A, Kondorosi E. 1999. The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO Journal 18: 4476-4484.
8. Cheng X, Wen J, Tadege M, Ratet P, Mysore KS. 2011. Reverse genetics in Medicago truncatula using Tnt1 insertion mutants. Methods in Molecular Biology 678: 179-190.
9. Coque L, Neogi P, Pislariu C, Wilson KA, Catalano C, Avadhani M, Sherrier DJ, Dickstein R. 2008. Transcription of enod8 in Medicago truncatula nodules directs enod8 esterase to developing and mature symbiosomes. Molecular Plant-Microbe Interactions 21: 404-410.
10. Cosson V, Durand P, d'Erfurth I, Kondorosi A, Ratet P. 2006. Medicago truncatula transformation using leaf explants. Methods in Molecular Biology 343: 115-127.
11. Ehrhardt DW, Atkinson EM, Long SR. 1992. Depolarization of alfalfa root hair membrane potential by Rhizobium meliloti nod factors. Science 256: 998-1000.
12. El Yahyaoui F, Kuster H, Ben Amor B, Hohnjec N, Puhler A, Becker A, Gouzy J, Vernie T, Gough C, Niebel A et al. 2004. Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiology 136: 3159-3176.
13. d'Erfurth I, Cosson V, Eschstruth A, Lucas H, Kondorosi A, Ratet P. 2003. Efficient transposition of the Tnt1 tobacco retrotransposon in the model legume Medicago truncatula. Plant Journal 34: 95-106.
14. Garcia J, Barker DG, Journet EP. 2006. Seed storage and germination. In: Mathesius U, Journet EP, Sumner LW, eds. The Medicago truncatula handbook. ISBN 0-9754303-1-9. URL: http://www.noble.org/MedicagoHandbook/.
15. Haag AF, Baloban M, Sani M, Kerscher B, Pierre O, Farkas A, Longhi R, Boncompagni E, Herouart D, Dall'angelo S et al. 2011. Protection of Sinorhizobium against host cysteine-rich antimicrobial peptides is critical for symbiosis. PLoS Biology 9: e1001169.
16. Hakoyama T, Niimi K, Watanabe H, Tabata R, Matsubara J, Sato S, Nakamura Y, Tabata S, Jichun L, Matsumoto T et al. 2009. Host plant genome overcomes the lack of a bacterial gene for symbiotic nitrogen fixation. Nature 462: 514-517.
17. Hakoyama T, Niimi K, Yamamoto T, Isobe S, Sato S, Nakamura Y, Tabata S, Kumagai H, Umehara Y, Brossuleit K et al. 2012. The integral membrane protein SEN1 is required for symbiotic nitrogen fixation in Lotus japonicus nodules. Plant and Cell Physiology 53: 225-236.
18. 2 fixation: laboratory and field evaluation. Plant Physiology 43: 1185-1207.
19. He J, Benedito VA, Wang M, Murray JD, Zhao PX, Tang Y, Udvardi MK. 2009. The Medicago truncatula gene expression atlas web server. BMC Bioinformatics 10: 441.
20. Heinz DW, Essen LO, Williams RL. 1998. Structural and mechanistic comparison of prokaryotic and eukaryotic phosphoinositide-specific phospholipases C. Journal of Molecular Biology 275: 635-650.
21. Hoffmann B, Trinh TH, Leung J, Kondorosi A, Kondorosi E. 1997. A new Medicago truncatula line with superior in vitro regeneration, transformation, and symbiotic properties isolated through cell culture selection. Molecular Plant-Microbe Interactions 10: 307-315.
22. Hohnjec N, Lenz F, Fehlberg V, Vieweg MF, Baier MC, Hause B, Küster H. 2009. The signal peptide of the Medicago truncatula modular nodulin Mtnod25 operates as an address label for the specific targeting of proteins to nitrogen-fixing symbiosomes. Molecular Plant-Microbe Interactions 22: 63-72.
23. Iantcheva A, Chabaud M, Cosson V, Barascud M, Schutz B, Primard-Brisset C, Durand P, Barker DG, Vlahova M, Ratet P. 2009. Osmotic shock improves Tnt1 transposition frequency in Medicago truncatula cv jemalong during in vitro regeneration. Plant Cell Reporter 28: 1563-1572.
24. Kinoshita N, Ooki Y, Deguchi Y, Chechetka SA, Kouchi H, Umehara Y, Izui K, Hata S. 2004. Cloning and expression analysis of a mapkkk gene and a novel nodulin gene of Lotus japonicus. Bioscience Biotechnologies Biochemistry 68: 1805-1807.
25. Kondorosi E, Banfalvi Z, Kondorosi A. 1984. Physical and genetic analysis of a symbiotic region of Rhizobium meliloti: identification of nodulation genes. Molecular and General Genetics 193: 445-452.
26. Krall L, Wiedemann U, Unsin G, Weiss S, Domke N, Baron C. 2002. Detergent extraction identifies different Virb protein subassemblies of the type IV secretion machinery in the membranes of Agrobacterium tumefaciens. Proceedings of the National Academy of Sciences, USA 99: 11405-11410.
27. Kumagai H, Hakoyama T, Umehara Y, Sato S, Kaneko T, Tabata S, Kouchi H. 2007. A novel ankyrin-repeat membrane protein, IGN1, is required for persistence of nitrogen-fixing symbiosis in root nodules of Lotus japonicus. Plant Physiology 143: 1293-1305.
28. Lelandais-Briere C, Naya L, Sallet E, Calenge F, Frugier F, Hartmann C, Gouzy J, Crespi M. 2009. Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21: 2780-2796.
29. Leong SA, Williams PH, Ditta GS. 1985. Analysis of the 5' regulatory region of the gene for delta-aminolevulinic acid synthetase of Rhizobium meliloti. Nucleic Acids Research 13: 5965-5976.
30. Liu J, Miller SS, Graham M, Bucciarelli B, Catalano CM, Sherrier DJ, Samac DA, Ivashuta S, Fedorova M, Matsumoto P et al. 2006. Recruitment of novel calcium-binding proteins for root nodule symbiosis in Medicago truncatula. Plant Physiology 141: 167-177.
31. Maunoury N, Redondo-Nieto M, Bourcy M, Van de Velde W, Alunni B, Laporte P, Durand P, Agier N, Marisa L, Vaubert D et al. 2010. Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two transcriptome-switches. PLoS ONE 5: e9519.
32. Meade HM, Long SR, Ruvkun GB, Brown SE, Ausubel FM. 1982. Physical and genetic characterization of symbiotic and auxotrophic mutants of Rhizobium meliloti induced by transposon Tn5 mutagenesis. Journal of Bacteriology 149: 114-122.
33. Meckfessel MH, Blancaflor EB, Plunkett M, Dong Q, Dickstein R. 2012. Multiple domains in Mtenod8 protein including the signal peptide target it to the symbiosome. Plant Physiology 159: 299-310.
34. Mergaert P, Uchiumi T, Alunni B, Evanno G, Cheron A, Catrice O, Mausset AE, Barloy-Hubler F, Galibert F, Kondorosi A et al. 2006. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proceedings of the National Academy of Sciences, USA 103: 5230-5235.
35. Michell RH. 2011. Inositol and its derivatives: their evolution and functions. Advances in Enzyme Regulation 51: 84-90.
36. Mitra RM, Long SR. 2004. Plant and bacterial symbiotic mutants define three transcriptionally distinct stages in the development of the Medicago truncatula/Sinorhizobium meliloti symbiosis. Plant Physiology 134: 595-604.
37. Moreau S, Verdenaud M, Ott T, Letort S, de Billy F, Niebel A, Gouzy J, de Carvalho-Niebel F, Gamas P. 2011. Transcription reprogramming during root nodule development in Medicago truncatula. PLoS ONE 6: e16463.
38. Nicholson RL, Hammerschmidt R. 1992. Phenolic compounds and their role in disease resistance. Annual Review of Phytopathology 30: 369-389.
39. Oldroyd G. ED, Murray JD, Poole PS, Downie JA. 2011. The rules of engagement in the legume-rhizobial symbiosis. Annual Review of Genetics 45: 119-144.
40. Orosz L, Svab Z, Kondorosi A, Sik T. 1973. Genetic studies on rhizobiophage 16-3. I. Genes and functions on the chromosome. Molecular General Genetics 125: 341-350.
41. Penmetsa RV, Cook DR. 1997. A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275: 527-530.
42. Pislariu CI, Dickstein R. 2007. An IRE-like AGC kinase gene, MtIRE, has unique expression in the invasion zone of developing root nodules in Medicago truncatula. Plant Physiology 144: 682-694.
43. Pislariu CI, Murray J, Wen J, Cosson V, Duvvuru Muni RR, Wang M, Benedito V, Andriankaja A, Cheng X, Torres Jerez I et al. 2012. A Medicago truncatula tobacco-retrotransposon (Tnt1)-insertion mutant collection with defects in nodule development and symbiotic nitrogen fixation. Plant Physiology 159: 1686-1699.
44. Rakocevic A, Mondy S, Tirichine L, Cosson V, Brocard L, Iantcheva A, Cayrel A, Devier B, Abu El-Heba GA, Ratet P. 2009. MERE1, a low-copy-number copia-type retroelement in Medicago truncatula active during tissue culture. Plant Physiology 151: 1250-1263.
45. Ramirez M, Graham MA, Blanco-Lopez L, Silvente S, Medrano-Soto A, Blair MW, Hernandez G, Vance CP, Lara M. 2005. Sequencing and analysis of common bean ESTs. Building a foundation for functional genomics. Plant Physiology 137: 1211-1227.
46. Redondo-Nieto M, Pulido L, Reguera M, Bonilla I, Bolanos L. 2007. Developmentally regulated membrane glycoproteins sharing antigenicity with rhamnogalacturonan II are not detected in nodulated boron deficient Pisum sativum. Plant, Cell & Environment 30: 1436-1443.
47. Rosenberg C, Boistard P, Denarie J, Casse-Delbart F. 1981. Genes controlling early and late functions in symbiosis are located on a megaplasmid in Rhizobium meliloti. Molecular General Genetics 184: 326-333.
48. Samac DA, Penuela S, Schnurr JA, Hunt EN, Foster-Hartnett D, Vandenbosch KA, Gantt JS. 2011. Expression of coordinately regulated defence response genes and analysis of their role in disease resistance in Medicago truncatula. Molecular Plant Pathology 12: 786-798.
49. Scholte M, d'Erfurth I, Rippa S, Mondy S, Cosson V, Durand P, Breda C, Trinh H, Rodriguez-Llorente I, Kondorosi E et al. 2002. T-DNA tagging in the model legume Medicago truncatula allows efficient gene discovery. Molecular Breeding 10: 203-215.
50. Starker CG, Parra-Colmenares AL, Smith L, Mitra RM, Long SR. 2006. Nitrogen fixation mutants of Medicago truncatula fail to support plant and bacterial symbiotic gene expression. Plant Physiology 140: 671-680.
51. Suganuma N, Yamamoto A, Itou A, Hakoyama T, Banba M, Hata S, Kawaguchi M, Kouchi H. 2004. cDNA macroarray analysis of gene expression in ineffective nodules induced on the Lotus japonicus sen1 mutant. Molecular Plant-Microbe Interactions 17: 1223-1233.
52. Tadege M, Wen J, He J, Tu H, Kwak Y, Eschstruth A, Cayrel A, Endre G, Zhao PX, Chabaud M et al. 2008. Large-scale insertional mutagenesis using the Tnt1 retrotransposon in the model legume Medicago truncatula. Plant Journal 54: 335-347.
53. Timmers AC, Auriac MC, Truchet G. 1999. Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126: 3617-3628.
54. Timmers AC, Soupene E, Auriac MC, de Billy F, Vasse J, Boistard P, Truchet G. 2000. Saprophytic intracellular rhizobia in alfalfa nodules. Molecular Plant-Microbe Interactions 13: 1204-1213.
55. Van de Velde W, Guerra JC, De Keyser A, De Rycke R, Rombauts S, Maunoury N, Mergaert P, Kondorosi E, Holsters M, Goormachtig S. 2006. Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiology 141: 711-720.
56. Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, Farkas A, Mikulass K, Nagy A, Tiricz H et al. 2010. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327: 1122-1126.
57. Vasse J, de Billy F, Camut S, Truchet G. 1990. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. Journal of Bacteriology 172: 4295-4306.
58. Vasse J, de Billy F, Truchet G. 1993. Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. The Plant Journal 4: 555-566.
59. Vinardell JM, Fedorova E, Cebolla A, Kevei Z, Horvath G, Kelemen Z, Tarayre S, Roudier F, Mergaert P, Kondorosi A et al. 2003. Endoreduplication mediated by the anaphase-promoting complex activator ccs52a is required for symbiotic cell differentiation in Medicago truncatula nodules. Plant Cell 15: 2093-2105.
60. Wang D, Griffitts J, Starker C, Fedorova E, Limpens E, Ivanov S, Bisseling T, Long S. 2010. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327: 1126-1129.
61. Weber SS, Ragaz C, Hilbi H. 2009. Pathogen trafficking pathways and host phosphoinositide metabolism. Molecular Microbiology 71: 1341-1352.
62. Welchen E, Gonzalez DH. 2005. Differential expression of the Arabidopsis cytochrome c genes cytc-1 and cytc-2. Evidence for the involvement of tcp-domain protein-binding elements in anther- and meristem-specific expression of the cytc-1 gene. Plant Physiology 139: 88-100.
63. Young ND, Debelle F, Oldroyd GE, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H et al. 2011. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: 520-524.